Mosquito Systematics Vol. Lo(3) 1978 301 Comparative Structure of The
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Mosquito Systematics vol. lO(3) 1978 301 Comparative Structure of the Labiohypopharynx of Fourth Stage Mosquito Larvae (Diptera: Culicidae), with Comments on Larval Morphology, Evolution and Feeding Habits* Ralph E. Harbach Department of Entomology North Carolina State University Raleigh, North Carolina 27650 ABSTRACT. The labiohypopharynges of 62 species of fourth stage culicid larvae representing 3 genera of the Dixinae, 2 of the Chaoborinae and all but one (Fica%ia) of the 34 genera recognized by Knight and Stone (1977) have been studied with the light and scanning electron microscopes. The structure of the labiohypopharynx is described and illustrated for at least one species of each genus examined. Phylogenetic relationships are discussed in regard to larval morphology and feeding behavior. INTRODUCTION This paper concludes a series of comparative studies on the mouthparts of fourth stage culicid larvae. Knight (1971) examined the anatomy of the mandi- bles, determined the homologies of the mandibular substructures and developed a structural terminology "suitable for use in taxonomic studies." A similar study was conducted on the maxillae by Knight and Harbach (1977). The comparative examination of the labiohypopharynx made by Harbach and Knight (1977b) paved the way for the present paper. Although the structural interpretation presented herein is basically the same as that given by these authors, a new terminology has been devised which reflects a more refined in- terpretation of structure and conforms more closely to that applied to other insects. The references cited by Harbach and Knight should be consulted for a comprehensive introduction to the literature on the morphology of the labio- hypopharynx. Although Montschadsky (1936), Surtees (1959) and Harbach (1977) have out- lined certain evolutionary trends based on correlations between mouthpart struc- ture and feeding habit, the evolution of culicid larvae is still a much vexed question. In order to shed additional light on larval phylogeny, evolutionary relationships which I have derived from the aforementioned series of studies, as well as observations made on other aspects of larval morphology, are set forth in the discussion. MATERIALS AND METHODS Light and scanning electron microscope investigations were conducted on the labiohypopharynges of alcohol-preserved fourth stage larvae. Material for *This publication was supported in part by NIH Grant LM02787 to Kenneth L. Knight from the National Library of Medicine. 302 examination under the light microscope was prepared and mounted on glass slides according to the procedures of Wirth (1961) and Knight (1971). For the scanning electron microscope, heads were Freon critical-point-dried and mounted anterior end up on aluminum stubs. Once secured, the median labral plate, palatum, an- tennae, mandibles and maxillae were carefully removed from each head in order that the topography of the labiohypopharynx could be examined without obstruc- tion. The labiohypopharynges of one to several larvae were prepared for both the light and scanning electron microscopes. Concerning the figures, each drawing depicts an anterior or near anterior aspect of a labiohypopharynx with its dorsal extremity uppermost. All scale lines are equal to 0.05 mm. The species are grouped into subfamilies and tribes, otherwise the linear order of the taxa has no phylogenetic import. Species stu- died in addition to those illustrated are listed in an appendix. Following Edwards (1932), the family Culicidae is considered to include the Dixinae and Chaoborinae. The taxa constituting Edwards' subfamily Culicinae, however, are recognized here as belonging to the subfamilies Anophelinae, Culi- cinae and Toxorhynchitinae of Knight and Stone (1977). The tribes are those of Belkin (1962). OBSERVATIONS The labium of generalized insects is divided into a proximal postlabium comprising the submentum and mentum and a distal prelabium comprising the pre- mentum, glossae, paraglossae and the labial palpi. In most nematocerous larvae the postlabium has been largely incorporated into the ventral surface of the head capsule (nematocerous larvae are basically prognathous) with only the dis- tal portion of the mentum projecting beyond the anterior margin as a dentate lobe or ridge. The prelabium has united with the hypopharynx to form the compo- site tabiohypopharynx (LbHy). In culicid larvae the labiohypopharynx is attach- ed to the head between the mouth and the dorsomerrtwn (Dm), a transverse subdivi- sion of the mentum found in both culicid (Laffoon and Knight 1973) and chironomid larvae (Saether 1971), where it forms the protruding posterior wall of the pre- oral cavity (Figs. 1,2). The component parts of the labiohypopharynx, the dor- sal hypopharynx (Hy) and the ventral pretabiwn, are joined and supported dorsally by the cibaria2 bars (CB) extending from lateral areas of the cranium. Ventrally the labiohypopharynx is reflected into the mentum at the base of the dorsomentum (Figs. 1,2). Hypopharynx The fleshy hypopharyngeal lobe, often strengthened internally by a sclero- tized hypopharyngea2bar (HUB) (see e.g., Fig. 16), is separated from the scle- rotized prelabium by a slitlike saZ<vary meatus (SM) (Figs. 3,4,39) which is readily visible only with the scanning electron microscope (see the equivalent salivary slit in the lateral aspects of the labiohypopharynges figured by Harbach and Knight 1977b). The salivary orifice opens into the floor of the salivary meatus and is often seen in light microscope preparations. Mosquito Systematics Vol. lO(3) 1978 303 In most Culicinae the hypopharynx bears a pair of earlike lobes, the super- ~inquae (Sl) (see e.g., Figs. 9,13,28,31). These are often imperceptible when observed with the light microscope owing to their membranous nature. As in generalized insects, the superlinguae have united with the median Z~?Z@U (L) to form the definitive hypopharynx. The adoral surface of the hypopharynx of Zeugnomy&z bears a row of branched cuticular processes (Fig. 23) not unlike the "dichotomous bristles' which occur on the hypopharynx of certain simuliid larvae (Craig 1977). The labiohypopharynx of dixine larvae is unique in that the lateral sides of the hypopharyngeal com- ponent support a pair of denticulate tritural surfaces, the ~~popharyngeai!Mae (HyM) (Figs. 3,4). Prelabium The prelabial component of the labiohypopharynx is comprised chiefly of the labial prementtmt, and it is probable that a pair of extrinsic muscles which originate on the ventral cranial wall and insert laterally on often indisting- uishable prementat apodemes(PAP) (see e.g., Figs. 5,14,24,34) is one of two pairs of tentorio-premental muscles found in generalized insects. The central region of the prementum is commonly elevated and bears a variously developed collection of usually strongly sclerotized toothed or toothlike projections which encompass a pair of oval membranous areas. As has been suggested by other authors (Christophers 1960; Chaudonneret 1962), the membranous areas represent vestigial ZabiaZ patpi (LP). Separating the palpi in the Anophelinae and cer- tain Culicinae is a cusped tonguelike structure which seemingly corresponds to the fused glossae and paraglossae, the ZiquZa (Lg), of many other insects, LiguZa. The anopheline ligula (Figs. 5-7) strongly resembles the "ligula" (Saether 1971) of certain chironomid larvae (see the figures of Johannsen 1937). In many culicine larvae, notably those of the genera CuZex (Fig. 11) and Aedes (Fig. 27), the ligula is a recumbent troughlike structure which bears resembl- ance to the "ligula" of simuliid larvae (Craig 1977). In Paradkca, toxorhyn- chitine, and some culicine larvae, including most Sabethini, the ligula is un- recognizably fused with some of the toothlike elements of the prementum (see below). Labia2 paLpi. Each labial palpus commonly bears four sensory peglike structures (yin 1970), Labial pazpaz sensoria 1-4 (LPS , LPS2, LPS , LPS4), which are struc- turally similar to chemoreceptors known to &ave a gusta 2 ory function in other insects. Sensoria 1 and 2 often arise from a commonpedicel (see e.g., Figs. 25,37). Located on each side of the ligula in anopheline larvae is a scale- or leaflike process. These processes correspond exactly to the "paraglossae" (Saether 1971) of certain chironomid larvae. Das (1937), however, maintains that the paraglossae and glossae "generally form a single lobe" in larval in- sects. Since the structures arise from the labial palpi and appear to have an ill-defined socket, they are considered here as Zabiat pazpaz sensoria 5 (LPS5) (Figs. 5,6). 304 Prementum. In general, the most conspicuous feature of the culicid prementum is the intricate assemblage of toothlike processes which subtend the dorsal and lateral margins of the labial palpi. In the generalized condition exemplified by Opifea: fuscus (Fig. 21), these processes can be conveniently subdivided into three groups: 1) the bilaterally paired prementat teeth comprising (a) an inter- connected group of ZateraZ pwmentaZ teeth (LPT) which flank the labial palpi, and (b) a prementaz denta arch @DA) which curves around the dorsal margin of each palpus and is united with the base of the ligula; 2) a cluster of premental CUSPS (PCu) located centrally between the premental dental arches; and 3) a patch of numerous peglike processes, a prementai! maZa (PM), borne on each slop- ing dorsolateral surface adjacent to the lateral premental teeth. The premental teeth are weakly developed in dixine and anopheline larvae